Article

Nonmonotonic Synaptic Excitation and Imbalanced Inhibition Underlying Cortical Intensity Tuning

Guangying K. Wu,¹,⁴ Pingyang Li,¹ Huizhong W. Tao,¹,³ and Li I. Zhang¹,²,^∗

¹Zilkha Neurogenetic Institute, University of Southern California, Los Angeles, California 90033
²Department of Physiology and Biophysics, University of Southern California, Los Angeles, California 90033
³Department of Ophthalmology, Keck School of Medicine, University of Southern California, Los Angeles, California 90033
⁴Neuroscience Graduate Program, University of Southern California, Los Angeles, California 90033

∗Corresponding author
Li I. Zhang
liizhang@usc.edu

Summary

Intensity-tuned neurons, characterized by their nonmonotonic response-level function, may play important roles in the encoding of sound intensity-related information. The synaptic mechanisms underlying intensity tuning remain unclear. Here, in vivo whole-cell recordings in rat auditory cortex revealed that intensity-tuned neurons, mostly clustered in a posterior zone, receive imbalanced tone-evoked excitatory and inhibitory synaptic inputs. Excitatory inputs exhibit nonmonotonic intensity tuning, whereas with tone intensity increments, the temporally delayed inhibitory inputs increase monotonically in strength. In addition, this delay reduces with the increase of intensity, resulting in an enhanced suppression of excitation at high intensities and a significant sharpening of intensity tuning. In contrast, non-intensity-tuned neurons exhibit covaried excitatory and inhibitory inputs, and the relative time interval between them is stable with intensity increments, resulting in monotonic response-level function. Thus, cortical intensity tuning is primarily determined by excitatory inputs and shaped by cortical inhibition through a dynamic control of excitatory and inhibitory timing.